Performance and egg quality of light laying hens fed with canthaxanthin and marigold flower extract

 

 

K.M. Maia^{I, #}; D.O. Grieser^II; A.P.S. Ton^III; D.R. Aquino^I; M.T.F. Paulino^I; J.B. Toledo^I; S.M. Marcato^I

^IDepartment of Animal Science, State University of Maringá, Colombo Avenue, 1590, Zip Code 87.020-900, Maringá, Paraná, Brazil
^IIFederal University of South and Southeast of Pará, Institute of Studies of Humid Tropics. Xinguara, Para, Brazil
^IIIFederal University of Mato Grosso, Institute of Agrarian and Environmental Sciences, Sinop, Mato Grosso, Brazil

 

 

---

ABSTRACT

The aim of this study was to determine the best level of inclusion of natural (marigold flower extract) and synthetic (canthaxanthin) pigments in the diet of light laying hens from 75 to 85 weeks old in terms of effects on performance, egg quality, and economic viability of production. A total of 288 laying hens were used in a completely randomized design, with a 4 x 4 factorial arrangement, with four levels of marigold flower extract (2.10; 2.40; 2.70; 3.00 ppm) and four of canthaxanthin (0. 40; 0.70; 1.00; 1.30 ppm), with three replications and six hens per experimental unit. The feed conversion by mass of eggs, egg mass, and egg laying rate showed linear improvement with the inclusion of canthaxanthin. The yolk index showed a quadratic effect with the inclusion of marigold and canthaxanthin, presenting a better estimate with diets containing 2.60 ppm/kg of marigold feed and 0.95 ppm/kg of canthaxanthin feed. The percentage of yolk and the Haugh unit increased linearly with the rising levels of marigold, whereas the percentage of albumen decreased linearly. In the evaluation of the YolkFan DSM® and the redness/yellowness, chroma (a*) presented a quadratic effect for the inclusion of marigold (2.73 and 2.80 ppm/kg of feed) and linear increase with canthaxanthin. It was concluded that the best yolk index was with 2.60 ppm/kg marigold flower extract and 0.95 ppm/kg canthaxanthin in the diet of light laying hens from 75 to 85 weeks old.

Key words: pigments, xanthophylls, yolk colour, yolk fan

---

 

 

Introduction

The diets of laying hens are based mostly on corn and soybean meal. In addition to being an energy source, corn contains xanthophylls, which are responsible for the pigmentation of the yolks, skins, and beaks of birds (Curvelo et al., 2009). However, a significant reduction may occur in yolk colour (Carneiro, 2013) when this cereal is stored and processed improperly.

Carotenoid supplementation in the diet of laying birds has been used to intensify the colour of the egg yolk. Not only does it increase the amount of pigment in the yolk (Papadopoulos et al., 2019), but it has benefits for human health, such as an attenuation of muscle degeneration (Zeheer, 2017), reduction in cardiovascular disease (Gammone et al., 2015), diminution of oxidative stress (Fiedor & Burda, 2014), and decrease in the risk of cancer (Mares-Perlman et al., 2002).

In Brazil, the natural pigments most commonly used in the production of poultry species such as broilers, laying hens, and laying quails include extract of marigold flower (Tagetes erecta), red pepper paprika (Capsicum annuum), and annatto (Bixa orellana). The most common synthetic pigment is canthaxanthin (Golabart et al., 2004; Fassani et al., 2019; Valentim et al., 2019).

The marigold flower is the only natural pigmentation that is sold as a source of lutein, which is used to intensify the yellow colour of the egg yolk (Volp et al., 2009). Canthaxanthin is a natural carotenoid that is present in some bird species. It is responsible for the red colour in flamingos, for example, and can be used in its synthetic form to feed broilers and laying hens to pigment the skin and egg yolk (Garcia et al., 2009).

To produce good quality eggs that are more economically viable, it is necessary to conduct research to improve the nutrition of laying hens and their products. The objective of this study was therefore to determine the best level of inclusion of natural pigments (marigold flower extract, yellow pigment) and synthetic (canthaxanthin, red pigment) in the diet of light laying hens from 75 to 85 weeks old on productive performance, the physical and chemical qualities of the eggs, and the economic viability of the enterprise.

 

Materials and Methods

The experiment was carried out at a laying hen farm called Granja Figueiredo, in the northwest of Paraná State, Brazil. The research followed all the rules proposed by the Ethics Committee on the Use of Animals (ECUA) from the State University of Maringá (UEM) (Protocol number 8244200418/2018).

A total of 288 light laying hens (commercial hens of the Hisex lineage) were used, 75 weeks old, with an average weight of 1.640 ± 0.224 kg. They had been raised until the beginning of the experiment in a conventional system, following the recommendations of the breeder manual, and were housed in the rearing and laying phases in conventional cages.

The experiment for laying hens extended from 75 to 85 weeks old (egg-laying phase), which was divided for analysis into three periods of 21 days. The hens were distributed in a completely randomized design, in a 4 x 4 factorial scheme, with four levels of marigold flower extract (2.10; 2.40; 2.70; 3.00 ppm), and four levels of canthaxanthin (0, 40; 0.70; 1.00; 1.30 ppm), with 16 treatments and three repetitions of six hens/experimental unit, totalling 48 experimental units. During the experiment, laying hens were housed in an open Californian-type aviary, with 2.00 m high ceilings, covered with clay tiles, opened at the upper part of the roof, and equipped with conventional laying cages (50 cm χ 45 cm χ 45 cm). They were laid out in simple rows with six hens per cage, trough-type feeders and nipple drinkers, with feed distribution and manual egg collection.

Water and feed were provided ad libitum, and the lighting programme was 16 hours of light throughout the experiment. The diets were based on corn, soybean meal, and wheat meal to meet the nutritional requirements of laying hens in the final laying stage, according to Rostagno et al. (2017), varying only in the inclusion of pigments in the diet (Table 1). Ambient temperature and relative humidity were recorded twice a day at 08h00 and 16h00, using two thermo-hygrometers, placed at the beginning and end of the aviary, and were the average of all periods, with a maximum ambient temperature of 28 °C and minimum of 18.97 °C and relative humidity of maximum 56% and minimum 26.44%.

Productive performance (feed intake, oviposition rate, egg mass (EM), feed conversion per dozen (FC, kg/dz) and egg mass (FC, g/g)) were evaluated throughout the experiment. The oviposition rate of housed birds was calculated by dividing the total number of eggs produced in the period by the number of birds, multiplied by 100. Laying hens and diets were weighed at the beginning and end of each cycle to determine bodyweight, feed consumption, and feed conversion. Weight gain was calculated as the difference between the initial and final weights, and feed consumption as the difference between the feed provided and that left over.

The laying rate was assessed by dividing the total number of eggs produced in the period by the number of hens, multiplied by 100. The egg mass was measured by dividing the total egg weight by the total number of hens in each unit. The feed conversion per dozen was calculated by dividing feed consumption by the number of dozens of eggs produced. The egg mass after feed conversion was measured by dividing feed consumption by the mass of eggs produced.

The average egg weight (EW) was determined by dividing the total egg weight on each of the last three days of each period by the number of weighed eggs. In the last three days of each period, three eggs per replication were used to evaluate specific gravity (SG), yolk index (YI), Haugh unit (HU), pigmentation of egg yolks by subjective Roche colorimetric fan and objective methods, components of the eggs, pH of egg white and egg yolk, and thickness of the eggshell.

Hamilton (1982) measured SG from the immersion of eggs in containers with saline solutions (densities of 1.065, 1.070, 1.075, 1.080, 1.085, 1.090, and 1.095). The height and diameter of the albumen and yolk were measured with a digital calliper (Harnder et al., 2008), which consisted of breaking the eggs into a smooth flat glass plate. The formula used to calculate the Haugh unit was

where H is the height of the albumen (HA) in millimetres, and W is the weight of the egg in grams (Haugh, 1937). A digital calliper was used to calculate YI, in which the height and width of the yolk were measured. These values were applied to the equation described by Sharp & Powell (1930),

where HY is the height of the yolk (mm), and WY is the width of the yolk.

The eggshells were dried out for 24 h at room temperature (22 °C), then placed in an oven for 72 h at 60 °C. Two points were selected in the centre-transversal area to measure the thickness of the shell with a micrometer with divisions of 0.01 mm (Lin etaí., 2004).

The colour of the egg yolk was assessed subjectively with the Roche yolk colour fan, which evaluates colour on a scale from 1 to 15, where 1 is the most depigmented and 15 is the most pigmented. The egg white, yolk, and albumen were weighed separately to determine egg components (Ahn et al., 1997). The pH of the egg white and yolk were measured with a digital pH meter (Instituto Adolfo Lutz,1985).

The colour of the egg yolk was analysed by an objective method by measuring these parameters: L*, which represents luminosity (L* = 0, black; L* = 100, white); a* and b*, which are the coordinates of the colours responsible for chromaticity (+ a * = red; - a * = green; + b * = yellow; - b * = blue) with a portable colorimeter (CR400m, Minolta), which was previously calibrated in black (0) and white (100), using D65 illuminant and a 10° observer's angle. To analyse the stability of the colour of the eggs, an egg was collected by replication during the first 21 days of the experiment, and the colour evaluation of the yolks was carried out subjectively using the Roche colour fan.

The statistical analysis of the data was performed with the SAS statistical program (SAS Inst. Inc., Cary, NC), according to the model:

where Y^ijki = variable measured in experimental unit k, fed with a diet containing level i of marigold flower extract and level j of canthaxanthin; bo = general constant;

bⁱ = linear regression coefficient as a function of the level of marigold flower extract;

Mⁱ = marigold flower extract content for laying hens (from 75 to 85 weeks old): M1 = 2.10 ppm; M2 = 2.40 ppm; M3 = 2.70 ppm and M4 = 3.00 ppm;

C^j = canthaxanthin content for laying hens (from 75 to 85 weeks old): C1 = 0.40 ppm; C2 = 0.70 ppm; C3 = 1.00 ppm and C4 = 1.30 ppm;

b² = linear regression coefficient as a function of canthaxanthin level;

b³ = quadratic regression coefficient as a function of marigold flower extract level;

b⁴ = quadratic regression coefficient as a function of canthaxanthin level;

b⁵ = linear regression coefficient as a function of the interaction between the level of marigold flower extract and the level of canthaxanthin;

FA = lack of adjustment of the regression model;

e^ijki = random error associated with each observation

Regression analyses of the levels of inclusion of marigold flower extract and canthaxanthin were performed and estimates of these levels were obtained using a quadratic model (Sakomura & Rostagno, 2016).

 

Results and Discussion

No interaction effect was observed between the levels of marigold and canthaxanthin flower extract on the variables, indicating that they acted independently (Tables 2, 3, 4, 5, and 6).

Feed consumption (g/g) improved linearly with the inclusion of canthaxanthin in the diet, whereas EM and PR showed an increasing linear effect for inclusion of canthaxanthin. The levels of marigold and canthaxanthin flower extract did not influence FI and FC (kg/dz) during the experiment. Yolk index showed a quadratic effect for the inclusion of marigold and canthaxanthin flower extract

The thickness of the shell and SG showed a decreasing linear effect with the inclusion of marigold and canthaxanthin flower extract. The variables, average egg weight (AEW) and the percentage of eggshell, showed a linear effect because of the inclusion of canthaxanthin in the feed, with this effect increased for AEW and decreased for the percentage of eggshell. The percentage of egg yolk and HU variables showed a linear effect with increasing levels of canthaxanthin. The percentage of albumen showed a linear reduction when the extract of the marigold flower was included. The levels of marigold and canthaxanthin flower extract did not influence the pH of albumen and yolk during the experiment.

Table 3 shows the regression equations for egg quality parameters of light hens aged between 75 and 85 weeks fed with marigold and canthaxanthin flower extracts.

The quadratic effect of the marigold flower extract produced a linear increase for canthaxanthin on the Roche colorimetric fan (LCR) and a* variables, indicating estimates of maximum yolk colour with 2.73 and 2.80 ppm/kg of the flower extract of marigold with increased levels of canthaxanthin. The content of marigold and canthaxanthin flower extract did not influence the variables L * and b * during the experiment. Pigments from marigold flower extract and canthaxanthin are classified in Brazil as sensory additives or substances that are added to animal feed to preserve, intensify colour, taste, and odour and modify their properties, without harming the nutritional value of the feed (IN N°13/2004 - Brazil, MAPA, 2004). Canthaxanthin may be considered provitamin (Beardsworth & Henández, 2003), because of its antioxidant properties and ability to be converted into vitamin A (Surai, 2003; Surai et al., 2006).

Several studies have analysed the effect of the addition of pigments to the diets of poultry (Garcia et al., 2002; Moeini et al., 2013; Sandeski, 2013; Fernandes, 2016; Fassani, 2019; Papadopoulos et al., 2019; Valentim et al., 2019). These authors claim that treatments containing synthetic and natural pigments do not influence the performance of the birds or the quality of the eggs. They merely commented on intensification of the colour of the egg yolk. However, in the present work, the authors observed that the variables of the productive performance of laying hens (FC (g/g), EM and PR) were influenced satisfactorily with the addition of marigold and canthaxanthin.

Sandeski (2013) added canthaxanthin and yellow pigmentation (lutein + zeaxanthin) to the diet of light laying hens in the egg-laying phase and observed that EW did not change because of the treatments. However, they observed that the supplementation of the diets of light laying hens from 90 to 103 weeks old with carotenoid additives based on red pepper (Capsicum annuum) and marigold flower extract did not have positive effects on their performance, but that EW increased.

Fernandes (2016) evaluated the use of vitamin E, selenium, and canthaxanthin in the diet of laying hens of 40 to 55 weeks and observed that the inclusion of 6 ppm canthaxanthin provided an increase in EW compared with the other treatments (vitamin E and selenium). The same result was found by Oliveira et al. (2017), who studied the addition of paprika extract and marigold flower extract to the diet of 160 light laying hens aged 95 weeks, and by Fassani et al. (2019), who evaluated the addition of commercial pigments based on canthaxanthin and annatto to the diet of light laying hens that were 55 weeks old.

The synthesis of pigments in the egg yolk begins with the processes of digestion and metabolism, which are similar to that of cholesterol in poultry. After they are consumed, they are digested in the form of fat droplets, which are emulsified by bile salts, and transformed into micelles (Parker, 1996). They are transported through the lipoproteins in the cell membrane and accumulate in the fat-rich tissues, then are deposited in the egg yolk (Pérez-Vendrell et al., 2001; Faehnrich et al., 2016; Vinus et al., 2018), interfering with its composition (Surai et al., 2001).

The inclusion of marigold flower extract (2.60 ppm/kg) influenced the percentage of the yolk, and 0.95 ppm/kg of canthaxanthin increased YI. These results may be related to the greater amount of carotenoids transferred to the yolk and to an increase in the components that compose it, such as proteins and lipids promoted by the absorption of pigments (Carneiro, 2013).

Specific gravity is important for producers, as this variable indicates the quality of the eggshell, which is easy to analyse quickly at low cost without damaging the product (Santos et al., 2016). Peebles & McDaniel (2004) and Silva (2004) consider that the SG of the eggs cannot be less than 1.080. They believe that values below this could cause costly losses for the producers. Variations in SG can occur because of porosity, the presence of cracks in the eggshells (Freitas et al., 2004), and the age of laying hens (Domingues & Faria, 2019).

Studies also indicate that the older the poultry, the lower the percentage of the eggshell and TS, because the shell does not increase in the same proportion as EW, because of the lower deposition of calcium carbonate per unit area (Oliveira & Oliveira, 2013), thus increasing the quantity and thickness of the pores in the eggshell (Domingues & Faria, 2019). This may be the reason that the higher the inclusion of canthaxanthin in the current study, the greater the EW and the lower the percentage of eggshell. These variables are linked to the external quality of the eggs, i.e., the higher the SG values, percentage of shell and TS, the better the quality of the eggs, and greater their resistance to breaking and cracking (Domingues & Faria, 2019).

Oliveira et al. (2017) evaluated the addition of natural pigments (red pepper paprika and marigold flower extract) to the diet of light laying hens at 95 weeks old and reported a decrease in the percentage of eggshells and TS. In the current study, the addition of pigments caused a decrease in TS and SG. This can be explained by Hirsch et al. (2007). They reported that the lutein and zeaxanthin, which are the carotenoids present in the marigold flower extract, inhibited the activity of the hormone, oestrogen, which inhibits the action of carbonic anhydrase (an enzyme that is responsible for the formation of the eggshell) (Benesch et al., 1944). This may result in eggs with a soft shell or without a shell.

The Haugh unit is the variable that is most commonly used to measure the quality of the albumen. It is a mathematical expression that correlates the weight of the egg with the height of the albumen. The higher this index, the better the quality of the eggs (Oliveira & Oliveira, 2013; Domingues & Farias, 2019). According to USDA (2000), eggs can be classified into excellent (100.0 to 72.0), high (71.0 to 60.0), medium (59.0 to 30.0), and low quality (29.0 to 00.0). The values in the present study varied between 73.45 (2.10 ppm of the marigold flower extract and 0.40 ppm of canthaxanthin) and 86.56 (3.00 ppm of the marigold flower extract and 0.40 canthaxanthin ppm), indicating that the eggs were of excellent quality.

Similar values for HU were observed by Rojas et al. (2015), who evaluated the addition of 30 g and 60 g of canthaxanthin + annatto extract in the diet of laying hens of HyLine Brown lineage from 34 to 45 weeks old. They observed that the addition of 30 g and 60 g canthaxanthin and annatto extract showed HU values of 82 and 86, respectively. Similar values were reported by Garcia et al. (2002) and Garcia et al. (2009).

The colour intensity of the yolk of laying hens depends on the amount of carotenoids consumed in the diet, because hens are not able to synthesize these pigments. The greater the consumption of food with a higher concentration of carotenoids, the greater the deposition in the yolk and concomitant intensity, to the point of saturating the colour, such that the addition of pigment to the diet no longer has an effect (Curvelo et al., 2009). Yolk deposition occurs in concentric layers. To obtain the most intense colouring, a combination of two pigments is needed, since the deposition of the egg yolk occurs in two phases.

Saturation is for the deposition of yellow carotenoids forming a base, which will present uniform deposition so that good saturation of the final colour occurs afterwards. After the deposition of the base (yellow), the second phase of pigmentation, which is the addition of red carotenoids, changes the tone (yellow) for the most reddish-orange colour. The combination of the pigments presenting these two colours is therefore more interesting when the objective is to increase the intensity of these two compounds (Fletcher & Hallo Ran, 1983). Sandeski (2013) confirmed that 15 days of yellow and red synthetic pigments are needed to achieve saturation. In Hammershoj et al. (2010), it took 14 days with various natural pigments in the diet of light laying hens. In the current study, it took an average of 18 days on the diets containing the various pigments for yolk colour saturation to occur.

The efficiency of yolk pigmentation depends on several factors, for example the amount of carotenoid ingested, the period of consumption of the additive (Curvelo et al., 2009), and the birds' ability to absorb the carotenoids in the diet (Amaya et al., 2013). It is therefore impossible to predict the pigmentation capacity of the additives accurately. Some authors have reported that synthetic pigments are more efficient than natural pigments in effective pigmentation of the yolk (Moura et al., 2011; Valentim et al., 2019). Inclusion of marigold flower at 2.73 ppm and canthaxanthin at 1.30 ppm in the current study showed an increase in the degree of yolk colour, reaching a score of 8 in the subjective LCR method, indicating the need to use the association of the two pigments for homogeneous yolk colouring.

Valentim et al. (2019) compared the use of paprika extract, marigold flower, and canthaxanthin in the diet of black laying hens (Avifran) at 60 weeks of age. The authors did not observe the influence of additives on the parameters of performance and quality of the eggs. A significant difference was observed only in the colour of the yolk, in which the inclusion of 0.045% canthaxanthin presented a greater average (12.62) according to the Roche colour fan, because the chemical capacity of canthaxanthin is greater than that of natural pigments. However, the inclusion of natural pigments showed satisfactory values, confirming that synthetic dye could be substituted, reducing the cost of production.

 

Conclusion

To obtain the best YI, the optimal inclusion level was 2,60 pp/kg of marigold flower extract and 0.95 ppm/kg of canthaxanthin in a diet based on corn, wheat, and soybean meal, in light laying hens from 75 to 85 weeks old.

 

Acknowledgements

The authors gratefully acknowledge the Brazilian National Council for Scientific and Technological Development (CNPq) for granting this research. The present work was also carried out with the support of the Coordination for the Improvement of Higher Education Personnel - Brazil (CAPES), for dissertations, theses, and other publications.

Authors' contributions

KMM, DOG, and SMM designed this experiment; KMM, DRA, MTFP, JBT, and DOG performed the animal experiments, measured, and acquired the data; KMM, DOG, and APST participated in result tabulation and statistics; KMM and SMM wrote the manuscript and revised it; DOG and SMM supervised all processes from performing the experiment to writing the manuscript. All authors read and approved the final manuscript.

Conflict of interest declaration

All authors declare that there are no conflicts of interest in the information provided in this paper.

 

References

Ahn, D.U., Kim, M. & Shu, H., 1997. Effect of egg size and strain and age of hens on the solids content of chicken eggs. Poult. Sci. 76, 914-919.         [ Links ]

Amaya, E., Becquet, P., Carné, S., Peris, S. & Miralles, P., 2013. Carotenoids in animal nutrition. Fefana, 1st edition. Fefana, 96.         [ Links ]

Beardsworth, P.M. & Hernández, J.M., 2003. Canthaxanthin is more than a safe carotenoid. Worlds Poult. Sci. 19, 14-15.         [ Links ]

Benech, R., Barron, N.S. & Mawson, C.A., 1944. Carbonic anhydrase, sulphonamides and shell formation in the domestic fowl. Fowl. Nature 153, 138-139.         [ Links ]

Brazil. MAPA - Ministério da Agricultura, Pecuária e Abastecimento, Instrução Normativa n°13 of November of 2004. Regulamento tecnico sobre aditivos para produtos destinados a alimentação animal. Diário Oficial da União, Brasília, DF, 2004.         [ Links ]

Carneiro J.S., 2013. Pigmentantes de gema: Novo método de avaliação de cor e caracterização da produtividade e saúde das poedeirs (thesis). Goiânia (GO): Universidade Federal de Goiás, Escola de Veterinária e Zootecnia, 107.         [ Links ]

Curvelo, E.R., Geraldo, A., Silva, L.M., Antos, T.A., Filho, J.A.V., Pinto, E.R.A., Oliveira, M.L.R. & Ferreira, C.B., 2009. Níveis de inclusão de extrato de urucum e açafrão em dietas para poedeiras semipesadas e seus efeitos sobre o desempenho e coloração da gema dos ovos. In: II Semana de Ciência e Tecnologia do IFMG campus Bambuí II Jornada Científica; Bambuí, Minas Gerais. Brasil.         [ Links ]

Domingues, C.H.F. & Faria, D.E., 2019. Qualidade interna e externa do ovo. In: D.E. Faria, D.E.F. Filho, M.R. Mazalli & M. Macari. Produção e processamento de ovos de poedeiras comerciais. Campinas: FACTA, pp 248-268.         [ Links ]

Faehnrich, B., Lukas, B., Humer, E. & Zebeli, Q., 2016. Phytogenic pigments in animal nutrition: Potentials and risks. Revisão. J. Sci. Food Agric. 96, 420-1430.         [ Links ]

Fassani, E.J., Abreu, M.T. & Silveira, M.M.B.M., 2019. Coloração da gema de ovo de poedeiras comercias recebendo pigmentante comercial na ração. Ci. Anim. Bras., 20, 1-10.         [ Links ]

Fernandes, M.O., 2016. Utilizaçãoo de vitamina E, selênio e cantaxantina na produção e qualidade de ovos de poedeiras comerciais. Dissertation. Santa Maria (RS): Universidade Federal de Santa Maria, Centro de Ciências Rurais.         [ Links ]

Fiedor, J. & Burda, K., 2014. Potential role of carotenoids as antioxidants in human health and disease. Nutrients 6(2), 466-88.         [ Links ]

Fletcher, D.L. & Hallo Ran, H.R., 1983. Egg yolk pigmenting properties of a marigold extract and paprika oleoresin in a practical type diet. Poult. Sci. 62,1205-1210.         [ Links ]

Freitas, E.R., Sakomura, N.K., Gonzalez, M.M. & Barbosa, N.A.A., 2004 Comparação de métodos de determinação da gravidade específica da gravidade específica de ovos de poedeiras comerciais. Pesq. Agropec. Bras. 39(5), 509512.         [ Links ]

Gammone, M.A., Riccioni, G. & D'Orazio, N., 2015. Carotenoids: Potential allies of cardiovascular health? Food Nutr. Res. 59, 26762.         [ Links ]

Garcia, E.A., Mendes, A.A., Pizzolante, C.C., Gonçalves, H.C., Oliveira, R.P. & Silva, M.A. 2002. Efeito dos níveis de Cantaxantina na dieta sobre o desempenho e qualidade dos ovos de poedeiras comerciais. Rev. Bras. Cie. Avíc. 4 (1), 1-7.         [ Links ]

Garcia, E.A., Molino, A.B., Berto, D.A., Pelícia, K., Osera, R.H. & Faitarone, A.B.G., 2009. Desempenho e qualidade de ovos de poedeiras comercias alimentadas com semente de urucum (Bixa Orellana L.) moida na dieta. Arq. Bras. Med. Vet. Zootec. 16(4), 689-697.         [ Links ]

Golabart, J., Sala, R., Rincón-Carruyo, X., Manzanilla, E.G., Vilà, B. & Gasa, J., 2004. Egg yolk color as affected by saponification of different natural pigmenting sources. J. Appl. Poultry Res. 13(2), 328-334.         [ Links ]

Hammershoj, M., Kidmose, U., Steenfeld, S., 2010. Deposition of carotenoids in egg yolk by short-term supplement of coloured carrot (Daucus carota) varieties as forage material for egg-laying hens. J. Sci. Food Agric. 90, 1163-1171.         [ Links ]

Hamilton, R.M.G., 1982. Methods and factors that affect the measurement of eggshell quality. Poult. Sci. 61, 2022-2039.         [ Links ]

Harnder, M.N.C., Brazaca, S.G.C., Savino, V.J.M. & Coelho, A.A.D., 2008. Efeito de Bixa orellana na alteração de características de ovos de galinhas. Cienc. Agrotec. 32(4), 1232-1237.         [ Links ]

Haugh, R.R., 1937. The Haugh unit for measuring egg quality. United States Egg Poultry Magazine 43, 552-555.         [ Links ]

Hirsch, K., Atzmon, A., Danilenko, M., Levy, J. & Sharoni, Y., 2007. Lycopene and other carotenoids inhibit estrogenic activity of 17p-estradiol and genistein in cancer cells. Breast Cancer Res. Treat. 104(2): 221-230.         [ Links ]

Instituto Adolfo Lutz. Normas analíticas do Instituto Adolfo Lutz. V.1: Métodos químicos e físicos para análise de alimentos. 3rd edition. IMESP, São Paulo. P. 533.         [ Links ]

Lin, H., Mertens, K., Kemps, B., Govaerts, T., Ketelaere, B., Baerdemaeker, J., Decuypere, E. & Buyse, J., 2004. New approach of testing the effect of heat stress on eggshell quality: Mechanical and material properties of eggshell and membrane. Br. Poult. Sci. 45(4), 476-482.         [ Links ]

Mares-Perlman, J.A., Millen, A.E., Ficek, T.L. & Hankinson, S.E., 2002. The body of evidence to support a protective role for lutein and zeaxanthin in delaying chronic disease. Overview. J. Nutr. 132, 518S-524S.         [ Links ]

Martin, N.B., Serra, R., Oliveira, M.D.M., Ângelo, J.A., Okawa, H., 1998. Sistema integrado de custos agropecuários - CUSTAGRI. Inf. Econ., 28(1), 7-28.         [ Links ]

Moeini, M.M., Ghazi, S.H., Sadeghi, S. & Malekizadeh, M., 2013. The effect of red pepper (Capsicum annuum) and marigold flower (Tageteserectus) powder on egg production, egg yolk color, and some blood metabolites of laying hens. Iranian J. Appl. Anim. Sci. 3(2), 301-305.         [ Links ]

Moura, A.M.A., Takata, F.N., Nascimento, G.R., Silva, A.F., Melo, T.V. & Cecon, P.R., 2011. Pigmentantes naturais em rações à base de sorgo para codornas japonesas em postura. R. Bras. Zootec. 40(11), 2443-2449.         [ Links ]

Oliveira, B.L. & Oliveira, D.D., 2013. Qualidade e tecnologia de ovos - Lavras: Ed. UFLA.         [ Links ]

Oliveira, M.C., Silva, W.D., Oliveira, H.C., Moreira, E.Q.B., Ferreira, L.O., Gomes, Y.S., & Sousa Junior, M.A.P., 2017. Paprika and/or marigold extracts in diets for laying hens. R. Bras. Saúde Prod. Anim. Salvador 18, 293-302.         [ Links ]

Papadopoulos, G.A., Chalvatzi, S., Kopecky, J., Arsenos, G. & Fortomaris, P.D., 2019. Effects of dietary fat source on lutein, zeaxanthin, and total carotenoids content of the egg yolk in laying hens during the early laying period, Br. Poult. Sci. 60(4), 431-438.         [ Links ]

Parker, R.S., 1996. Absorption, metabolism, and transport of carotenoids. The FASEB Journal 10(5), 542-551.         [ Links ]

Peebles, E.D. & McDaniel, C.D., 2004. A practical manual for understanding the shell structure of broiler hatching eggs and measurements of their quality. Office of Agricultural Communications, Division of Agriculture, Forestry, and Veterinary Medicine, Mississippi State University 1139, 16.         [ Links ]

Pérez-Vendrell, A.M., Hernandez, J.M., Llaurado, L., Schierle, J. & Brufau, J., 2001. Influence of source and ratio of xanthophyll pigments on broiler chicken pigmentation and performance. Poult. Sci. 80(3), 320-326.         [ Links ]

Rojas, V.V., Callacna, M.C. & Arnaiz, V.P., 2015. Uso de un aditivo a base de cantaxantina y extracto de achiote en dietas de gallinas de postura y su efecto sobre la coloración de la yema y la vida de anaquel del huevo. Sci. Agric. 6(3), 191-199.         [ Links ]

Rostagno, H.S., Albino, L.F.T., Donzele, J.L., Gomes, P.C., Oliveira, R.F., Lopes, D.C., Ferreira, A.S., Barreto, A.L.T. & Euclides, R.F., 2017. Tabelas Brasileiras para Aves e Suínos: Composição de Alimentos e Exigências Nutricionais. 4th edition. Viçosa/MG: UFV, 2017.         [ Links ]

Sakomura, N.K. & Rostagno, H.S., 2016. Métodos de pesquisa em nutrição de monogástricos. 2 ed., Jaboticabal: Funep.         [ Links ]

Sandeski, L.M., 2013. Otimização da pigmentação da gema do ovo. (Dissertation). Araçatuba (SP): Universidade Estadual Paulista, Faculdade de Medicina Veterinária de Araçatuba.         [ Links ]

Santos, J.S., Maciel, L.G., Seixa, V.N.C. & Araújo, J.A., 2016. Parâmetros avaliativos da qualidade física de ovos de codornas (Coturnix coturnix japônica) em função das características de armazenamento. R. Desafios 3(1), 54-67.         [ Links ]

SAS (Statistical Analyses System). Version 8.2. for Windows. Cary: 2001.         [ Links ]

Sharp, P.F. & Powell, C.K., 1930. Decrease in internal quality of hen's eggs during storage by the yolk. Industrial & Engineering Chemistry Research 22, 909- 910.         [ Links ]

Silva, F.H.A., 2004. Curso teórico-prático sobre técnicas básicas de avaliação de qualidade do ovo. Piracicaba: ESALQ.         [ Links ]

Surai, P.F., Speake, B.K. & Sparks, N.H.C., 2001. Carotenoids in avian nutrition and embryonic development. 1. Absorption, availability and levels in plasma and egg yolk. J. Poult. Sci. 38, 1-27.         [ Links ]

Surai, P.F., 2003. Natural antioxidants in avian nutrition and reproduction. Nottingham University Press, Nottingham.         [ Links ]

USDA (United States Department Of Agriculture), 2000. Egg-grading manual. Washington (75). http://www.ams.usda.gov/AMSv1.0/getfile?dDocName=STELDEV3004502; accessed April 2021.         [ Links ]

Valentim, J.K., Bittencourt, T.M., Lima, H.J.D., Moraleco, D.D., Tossuê, F.J.M., Silva, N.E.M., Vaccaro, B.C. & Silva, L.G., 2019. Pigmentantes vegetais e sintéticos em dietas de galinhas poedeiras negras. Boletim Indústria Animal 76, 1-9.         [ Links ]

Vinus, R.D., Dalal, R., Sheoran, N., Maan, N.S. &Tewatia, B.S., 2018. Potential benefits of herbal supplements in poultry feed: A review. J. Pharm. Inn., 7, 651-656.         [ Links ]

Volp, A.C.P., Renhe, I.R.T. & Stringueta, P.C., 2009. Pigmentos naturais bioativos. Alim. Nutr. 20(1), 157-16.         [ Links ]

Zaheer, K., 2017. Hen egg carotenoids (lutein and zeaxanthin) and nutritional impacts on human health: A review. CYTA - J. Food, 15(3), 474-487.         [ Links ]

 

 

Submitted 24 April 2021
Accepted 22 February 2022
Published 14 October 2022

 

 

# correspondence author: karinamaiaka@gmail.com